I

Adult Adult males females

Fig. 3.12 Sex differences in the prevalence of STDs. Bars represent mean prevalence of STDs in males and females, +1 SE, based on 19 estimates of STD prevalence in adults from 8 Old World primates. The difference in prevalence was statistically significant (matched pairs test, t18 = 2.49, P = 011, one-tailed). From Nunn and Altizer (2004), printed with permission of Cambridge University Press.

Adult Adult males females

Fig. 3.12 Sex differences in the prevalence of STDs. Bars represent mean prevalence of STDs in males and females, +1 SE, based on 19 estimates of STD prevalence in adults from 8 Old World primates. The difference in prevalence was statistically significant (matched pairs test, t18 = 2.49, P = 011, one-tailed). From Nunn and Altizer (2004), printed with permission of Cambridge University Press.

than females. In another study, Pettifer (1984) suggested that physiological differences between the sexes accounted for a higher prevalence of Physaloptera caucasica in males, although the author also noted that it could be due to sex differences in consumption of the arthropod intermediate hosts. In terms of STDs, a recent comparative test showed that prevalence was higher among females (Fig. 3.12, Nunn and Altizer 2004), as predicted by individual-based models showing increased biases in prevalence toward females as sexual selection increases (Thrall et al. 2000).

Thus, few consistent patterns in relation to sex have been documented in primates (Table 3.6, see also Solomon 1969), potentially because multiple factors operate in different directions. Comparative approaches are likely to offer the strongest tests of the factors that influence patterns of parasitism among the sexes (Moore and Wilson 2002), but to obtain sufficient sample sizes, such tests will require additional field studies that collect parasite data from individually recognizable males and females (e.g. Müller-Graf et al. 1996, 1997). Future studies should investigate additional host and parasite traits that drive patterns in unexpected directions. Encounter probabilities in particular are under-explored. For example, if females are more likely to seek protein by consuming insects, while larger-bodied males eat leaves, this could increase female exposure to parasites transmitted via intermediate hosts.

3.3.5 Ranging behavior, substrate use, and diet

3.3.5.1 Range use

Animals that inhabit larger areas, utilize a greater variety of habitats, or travel longer distances per day should encounter a greater variety of parasite species (Mohr and

Stumpf 1964; Nunn et al. 2003a). Alternatively, animals restricted to smaller areas could experience continual re-infection with parasites that accumulate in the habitat, particularly infectious stages of intestinal parasites that are shed in feces (Freeland 1976, 1980; Hausfater and Meade 1982; Stoner 1996). Thus, hosts with wide geographic ranges should harbor a greater diversity of many types of parasites, whereas hosts that defend a stable home range should experience more intense infections by parasites that accumulate in the environment (Freeland 1976).

Primate field researchers typically report three measures of ranging behavior: home range size, day journey length, and a variable derived from these two measures known as the "defensibility index" or D-index (Mitani and Rodman 1979). Home range size refers to the area covered by a group of primates, usually throughout the year. Within this range, a smaller area might actually be defended (Cheney 1987). Day journey length refers to the distance that a group (or individual) travels in a day, based on following the animals throughout their active period. Finally, the D-index measures the intensity of range use and is calculated by examining day journey length relative to the size of the home range, based on the assumption of a circular home range. Mitani and Rodman (1979) found that the D-index correlated positively with qualitative measures of territoriality across species of primates (see also Lowen and Dunbar 1994), indicating that animals were more likely to defend areas that are regularly utilized. The probability of re-infection with parasite infectious stages that build up and persist in the environment should correlate positively with this measure of range use intensity.

Few field or comparative studies of primates examined the effect of range use on parasitism. In their comparative studies of parasite species richness in primates, Nunn et al. (2003a) found that day range length correlated positively with the number of virus species reported in different primate hosts. Counter to predictions, however, a negative association between home range size and parasite species richness arose for some analyses (C. Nunn, unpublished data) and the D-index was positively correlated with helminth species richness (Nunn and Dokey, in review). Even fewer studies examined patterns within species, although a study of California meadow mice (Microtus californicus) found that mice with larger home ranges harbored more intense chigger infections (Mohr and Stumpf 1964).

Finally, use of specific parts of a home range could affect disease risk. Hausfater and Meade (1982) proposed that a troop of baboons at Amboseli altered their use of sleeping groves in response to infectious stages of parasites that accumulate in the soil below sleeping trees. Similarly, animals might modify ranging behavior to avoid fetid water sources, fecal contaminated soil, or other habitats that expose them to parasites (see Chapter 5).

3.3.5.2 Range overlap, territoriality, and dispersal

Increased contact between social groups should improve the ability of parasites to spread and establish in primate populations (Freeland 1976, 1979; Loehle 1995; Watve and Jog 1997; Wilson et al. 2003). Between-group contact might occur indirectly when group ranges coincide, as this provides a means for parasites to spread through contact with water or soil contaminated by other groups, or even through contact with dead animals from neighboring groups (Walsh et al. in review). The extent of range overlap varies greatly among primate species (Cheney 1987), and general predictions are that most measures of disease risk will increase with range overlap. Thus, a recent study of gorillas in the Kahuzi-Biega National Park found that home range overlap influenced the infection rate of individual gorilla hosts based on fecal samples of gut parasites (Eilenberger 1997). However, a preliminary comparative study of parasite richness in relation to primate home range overlap produced no significant results (Nunn and Dokey, in review). Future studies could investigate patterns of range overlap and parasitism to a greater extent in wild populations.

Animals dispersing from infected groups represents another route for parasites to spread through populations. This possibility was discussed by Freeland (1976), who suggested that animals might undergo a period of "social ostracism" before being allowed to enter a new group (see also Tutin 2000). Host dispersal should affect the spread of STDs, since this class of parasites requires intimate contact, and therefore host movement between groups should increase the establishment of STDs in a population (Thrall et al. 2000). For non-STDs, Freeland (1979) found that different groups of baboons (P. anubis) harbor more similar protozoa than do rainforest monkeys, and he suggested that this can be explained by the observation that individuals transfer between groups more commonly in baboons. As further testimony to this possibility, Barrett and Henzi (1998) noted that an unidentified pathogen was introduced to a new troop of baboons through transfer of an infected animal, and a disease similar to yaws was also likely to have spread through inter-troop transfer among baboons at Gombe (A. Collins, personal communication).

Finally, territoriality will likely reduce contact among neighboring groups, but in some cases it could also lead to aggressive interactions during territorial encounters, resulting in the spread of disease between groups (Loehle 1995). Many viruses are spread through territorial interactions in free-living carnivores, including rabies in foxes (White et al. 1995) and FeLV in feral cats (Pontier et al. 1998). Risks of pathogen transfer via aggressive contacts should increase in primate species with long canines that can pierce the skin and increase contact with blood or saliva (Tutin 2000). In a semi-free-ranging population of mandrills (Mandrillus sphinx), for example, SIV and STLV probably spread through biting associated with male intra-sexual competition (Nerrienet et al. 1998). Thus, patterns of disease risk with directly transmitted parasites should covary with canine size and quantitative measures of territoriality in comparative tests.

3.3.5.3 Geographic range size

All else equal, host species with larger geographic ranges—defined as the range of the species as a whole—should encounter more varied habitats and thus a wider diversity of parasites (Dritschilo et al. 1975; Price and Clancy 1983; Gregory 1990; Poulin and Morand 2004). Similarly, host species with larger geographic ranges are expected to overlap with a greater number of other host species, increasing the possibility of cross-species transmission events among sympatric hosts (Ezenwa 2003; Nunn et al. 2004). Parasites spread through fecal contamination of the environment, for example, could readily infect multiple host species in the same habitat, a situation that may be common for nonhuman primates with ranges that overlap with humans and domesticated animals (Chapter 7 and Nizeyi et al. 1999; Wallis and Lee 1999; Graczyk et al. 2001). Direct contact among different primate species also occurs when primates of different species form aggregations known as polyspecific associations, possibly for avoiding arthropod parasites (Freeland 1977) and other benefits (Waser 1987).

A number of parasite surveys in overlapping primate populations revealed shared parasite communities that could reflect the effects of overlapping geographic ranges (Meade 1984; McGrew et al. 1989a, b; Bakarr et al. 1991). For example, Landsoud-Soukate et al. (1995) compared patterns of prevalence in sympatric chimpanzees and gorillas in Lope Reserve, Gabon. They found that gorillas exhibited higher levels of parasitism with a variety of protozoa and helminths, as compared to chimpanzees, but six of the parasites (one may be commensal) occurred in both species of apes.

From a comparative perspective, Nunn et al. (2003a, 2004) found that geographic range size correlated with the richness of viruses and protozoa across anthropoid primates. Moreover, two measures of geographic range overlap among primate hosts explained additional variation in the diversity of generalist and specialist viruses, even after controlling for the correlated effect of geographic range size (Nunn et al. 2004). Host ranging variables should be explored in greater depth when more information becomes available on the global distribution of parasites in humans, domesticated species, and other mammals.

3.3.5.4 Terrestrial substrate use

Animals often defecate, cough, vomit, bleed, or urinate on the ground or low-lying substrates, and in so doing, they can disperse infective stages of parasites. Thus, it is reasonable to expect that terrestrial primates experience greater disease risk than arboreal primates (Nunn et al. 2000). Based on similar reasoning, Minette (1966) proposed that the general absence of Leptospira infections in New World monkeys reflects the more arboreal lifestyles of this group of primates, since this parasite is spread through contact with contaminated soil and water. Dunn (1968) even proposed that records of infection with trematodes and Leptospira could provide a useful proxy for the degree of arboreality for primate species whose behavior has not yet been studied!

Although this hypothesis is appealing, phylogenetically controlled cross-species studies thus far have generated no support for the role of substrate use as a factor that influences disease risk. Terrestriality failed to explain variation in leukocyte counts and spleen size after controlling for body mass (Nunn et al. 2000; Nunn 2002a,b); in fact, if any pattern is present, relative spleen size actually declined with increasing use of terrestrial substrates, in a direction opposite to predictions. The percentage of time terrestrial also showed no relationship with parasite species richness for three major groups of parasites (protozoa, viruses, and helminths), and similar results were obtained for categorical measures of terrestriality (arboreal, mixed, and terrestrial, Nunn et al. 2003a).

Several factors could explain a lack of association between disease risk and terres-triality. First, the basic assumption underlying the hypothesis, namely that arboreal species are protected from contaminated substrates, might be incorrect. Thus, Freeland (1980) found that mangabeys commonly defecated on branches used for arboreal locomotion, providing a means for intestinal parasites to spread even in an arboreal environment. Second, hypotheses concerning substrate use might be better tested using data on parasites that are known to have a strong environmental component to their transmission, such as contact with infectious stages in water. For example, Schistosoma have been reported mainly in ground-dwelling monkeys (e.g. Papio anu-bis, P. hamadryas, P. papio, and Cercopithecus aethiops; Else et al. 1982; McGrew et al. 1989a; Ghandour et al. 1995; Müller-Graf et al. 1997; Munene et al. 1998). This association makes sense because transmission of Schistosoma requires contact with a molluscan intermediate host—conditions that are less available in arboreal habitats

Fig. 3.13 Male chacma baboon walking through water at a research site in Botswana. Contact with slow moving or standing water could expose animals to intermediate stages of the trematode Schistosoma mansoni and parasitic worms, protozoa, viruses, and bacteria transmitted through water contaminated with animal feces or human sewage. Photo by D. Kitchen,

The Ohio State University.

Fig. 3.13 Male chacma baboon walking through water at a research site in Botswana. Contact with slow moving or standing water could expose animals to intermediate stages of the trematode Schistosoma mansoni and parasitic worms, protozoa, viruses, and bacteria transmitted through water contaminated with animal feces or human sewage. Photo by D. Kitchen,

The Ohio State University.

(e.g. Fig. 3.13). Finally, a commonly overlooked alternative hypothesis is that animals using both terrestrial and arboreal substrates might be exposed to more parasite species than those that specialize on only one of these substrate categories (Dunn 1968; Altmann 1974; Nunn et al. 2003a). These factors could be explored in future studies that compare populations or species that vary in their degree of arboreality.

Primates and other animals unintentionally ingest parasites by consuming contaminated food and water. Leaf-eating (folivorous) primates typically ingest larger volumes of food than frugivores and could therefore ingest more parasites whose infectious stages contaminate leaf material (Moore 2002). On the other hand, diets of frugivorous primates are often more varied, potentially leading to contact with a wider array of parasites, and in folivores, consumption of leaves with secondary compounds could reduce levels of intestinal parasites (e.g. Huffman 1997). Janzen (1978) even suggested that the general absence of protozoan parasites among folivorous primates could reflect a "steady flow of secondary compounds from the foliage that they eat" (p. 78).

Invertebrates, such as grubs and cockroaches, serve as intermediate hosts for trophically transmitted parasites, predicting increased diversity of these parasites among insectivorous primates. Consumption of ectoparasites during grooming should influence the distribution of ectoparasites among different primate hosts. Thus, Dunn (1968) proposed that insectivorous primates should more readily consume larger-bodied ectoparasites, possibly lowering the abundance of the larger ectoparasites among insect-eating primates.

Despite these probable links between diet and parasitism, few studies have demonstrated convincing evidence for effects of insectivory and folivory on primate exposure to infectious diseases. Two recent comparative studies found limited associations between parasite diversity and the percentages of different dietary components, with leaves positively correlated with the diversity of helminth species (particularly nematodes) in some analyses (Nunn et al. 2003a; Vitone et al. 2004), but generally non-significant for other parasite groups. In a comparative study of 23 mammals, however, basal metabolic rate exhibited a positive association with helminth richness, possibly because species with higher metabolic rates consume relatively more resources (Morand and Harvey 2000).

Other aspects of diet should influence disease risk, including prey specialization, cannibalism, coprophagy, and the need to drink water (rather than obtaining most fluids from fruit). Predation on other primates could serve as a source of new infections (Tutin 2000), as could cannibalism (e.g. Goodall 1986; Palombit 2000). Coprophagy, or the eating of feces, puts animals at risk of infection (or re-infection) with intestinal parasites if infectious stages are present in fresh feces, and this behavior has been observed in primates, including gorillas (Harcourt and Stewart 1978) and chimpanzees (Wrangham 1977; Goodall 1986; Krief et al. 2004). In gorillas, Harcourt and Stewart (1978) documented coprophagy in all age-sex classes. In most cases the animal ate its own dung. Moreover, coprophagy was associated with heavy rain and occurred more commonly at the end of a resting period. This behavior may serve many functions, including improved absorption of vitamins (see Harcourt and Stewart 1978) or re-ingestion of seeds passed through the intestinal tract (Krief et al. 2004). Primates that are in close proximity to humans have been observed to forage in garbage dumps, and this could expose them to infected meat or human waste (see Chapter 7 for additional details).

Finally, many primate species consume water from rivers, drinking holes, or lakes. These water sources provide opportunities for parasite infection. In Senegal, Guinea baboons (Papio papio) have been shown to carry S. mansoni (McGrew et al. 1989a), but green monkeys and patas monkeys are apparently not infected by this parasite (McGrew et al. 1989b). The authors suggested that levels of infection were higher in baboons because they more commonly used stagnant water sources (see also Altmann 1974). Green and patas monkeys, on the other hand, tended to drink from flowing or temporary water sources and showed no evidence of infection with schistosomes. Meade (1984) suggested that Amboseli baboons limit their visits to drinking holes in part to avoid moist soil that surrounds these holes and might serve as focal points for acquiring infections.

In summary, omnivorous primates with diverse diets of plants and animals might be exposed to a greater diversity of parasites (Dunn 1968), but insectivory could increase the transmission of certain types of parasites. Additional dietary behaviors, including preference for different types of water sources, coprophagy, and use of garbage dumps, should further affect disease risk in primates, although only a few links have been documented thus far. Since different populations of frugivores often have markedly different diets, future field and comparative research could provide new insights by comparing parasites among these populations.

3.3.6 Environmental factors and seasonality

Primate species, like other animals, experience dramatic variation in temperature, rainfall, and the abundance of resources. Seasonal reductions in rainfall could induce dietary stress as the availability of resources declines, increasing susceptibility to disease (Lloyd 1995; Beisel 2000; Nelson et al. 2002; Nelson 2004). These reductions could also force animals to share food and water resources with different social groups and even different species, potentially leading to more opportunities for the spread of parasites.

Vector-borne diseases are among the most likely to covary with environmental conditions (Dobson and Carper 1992; Harvell et al. 2002). Temperature and rainfall should affect arthropod vector distribution and abundance, parasite development, and parasite transmission rates (Kovats et al. 2001). Many vector-borne diseases are limited in geographic range by thermal constraints because parasites cannot complete development before the vectors die. Several vector-borne human pathogens that are also infectious to free-living primates have expanded their geographic ranges or become more prevalent in recent decades, including malaria, trypanosomiasis, yellow fever, and dengue (Gratz 1999; Lindgren et al. 2000).

A global analysis of human diseases found a strong association between parasite diversity and latitude, driven by climatic variables involving precipitation and temperature (Guernier et al. 2004, see also Chapter 8). Across primate species, a comparative analysis showed similar results, with increased parasite species richness among host species in the tropics (Fig. 3.14, Nunn et al. 2005). This pattern was strongest for protozoan parasites, perhaps due to the greater proportional representation of vector-borne parasites among protozoa recorded in primates (see Fig. 2.11). The pattern shown in Fig. 3.14 could also reflect a confounding influence of geographic range size, because when this variable was entered into the model, the latitudinal effect weakened.

Bioclimatographs that capture data on moisture and temperature have traditionally been used to predict outbreaks of gastrointestinal nematodes infecting livestock. These associations arise because intestinal macroparasites of terrestrial animals are often susceptible to variation in temperature and humidity at several stages of their life cycles (Gordon 1948; Smith 1990). In S. mansoni, for example, a 10° C increase in temperature can dramatically shorten development time by over two weeks (Gordon et al. 1934).

Rainfall can clear away pathogens, especially for arboreal primates exposed to contaminated vegetation. Thus, arboreal mangabeys (C. albigena) were found to use an area more intensively during the rainy season (Freeland 1980). Overall, however,

Log absolute median latitude

Fig. 3.14 Latitudinal gradients in protozoan parasite species richness. Points represent independent contrasts. Increases in median absolute latitude are associated with decreases in the size of the protozoan parasite community. In this plot, parasite species richness was measured as least-squares residuals following regression analysis of protozoan parasite richness and a measure sampling effort for each host species. From Nunn et al. 2005. Printed from Diversity and Distributions, with permission from Blackwell Publishing.

Log absolute median latitude

Fig. 3.14 Latitudinal gradients in protozoan parasite species richness. Points represent independent contrasts. Increases in median absolute latitude are associated with decreases in the size of the protozoan parasite community. In this plot, parasite species richness was measured as least-squares residuals following regression analysis of protozoan parasite richness and a measure sampling effort for each host species. From Nunn et al. 2005. Printed from Diversity and Distributions, with permission from Blackwell Publishing.

the parasite-related costs of increased moisture probably outweigh any potential benefits that rainfall might provide by removing parasites from the environment (Freeland 1980). Because many nematodes require strict moisture levels for development, Hausfater and Meade (1982) predicted that baboons would avoid contaminated sleeping sites more often in the rainy season than in the dry season—a prediction that was supported by their data. Similarly, several studies of arboreal primates showed a positive relationship between moist environments and intestinal macroparasite infections (Stuart et al. 1993, 1998; Stuart and Strier 1995; Stoner

1996). As noted above, intestinal parasite infections among howlers at La Selva (a wetter environment) were greater than among howlers at La Pacifica (a drier habitat). Furthermore, at La Selva, a river troop exhibited higher intensity of nematode infection than a forest group (Stoner 1996). Similar effects have been documented in terrestrial primate species, with nematode prevalence and intensity generally greater among baboons and chimpanzees at Gombe, as compared to populations inhabiting the drier conditions at Mt Assirik (McGrew et al. 1989a). Finally, in a recent comparative study of white blood cell counts in 33 primate species, lymphocyte and phagocyte concentrations correlated positively with rainfall (Semple et al. 2002).

Seasonal cycles can generate periodic transmission opportunities for some human and wildlife pathogens (Dowell 2001; Altizer et al. 2004). In chimpanzees, Huffman et al. (1997) found that the prevalence of infection by the nematode Oesophagostomum stephanosomum increased during the wet season in two years, with sharp peaks in egg production in infected individuals occurring 1-2 months after the onset of rains. Two other nematodes (Trichuris trichiura and Strongyloides fuelleborni) showed no seasonal variation in this population. In gorillas, Watts (1998) found that the incidence of respiratory infections (and deaths) were associated with annual periods of high rainfall, a pattern also suggested for geladas (Ohsawa and Dunbar 1984) and chimpanzees (Boesch and Boesch-Achermann 2000). Botfly infections also vary in abundance seasonally, being more common toward the end of the dry season (Smith 1977) and showing up to three cycles per year (Milton 1996). Meade (1984) found that spirurid nematode prevalence increased in the dry season, and Pettifer (1984) found that worm burdens in chacma baboons were higher during the wet season for Bertiella studeri and Oesophagostomum bifurcum, but the hookworm Trichostrongylus falculatus was more common in the dry season. Other studies have found no striking differences across seasons in the presence of macroparasites (intestinal parasites in chimpanzees, McGrew et al. 1989a; and schistosomes in baboons, Müller-Graf et al.

Additional effort should focus on examining environmental factors at regional and global scales using phylogenetic methods (Box 3.2) and geographic information systems (GIS), as discussed in Box 3.3. It is important to recognize that not all parasites will be sensitive to environmental factors or will show seasonal variation. Thus, some parasites, such as the nematode Trichuris, have thick shells that make them resistant to desiccation and may reduce the magnitude of the impact of seasonal fluctuations on survival (Meade 1984). Seasonal changes can also affect host susceptibility to infectious diseases (Combes 2000; Nelson et al. 2002; Nelson 2004). Thus, another potentially profitable direction would be to consider the links between dietary stress and disease susceptibility, particularly among primates that live in highly seasonal conditions, such as in Madagascar or desert habitats. Studies of rodents and humans suggest that immune systems are weakened during the winter (reviewed in Dowell 2001), and other environmental stressors or annual rhythms in immune function and reproduction could further weaken immunity and increase disease risk (Lloyd 1995; Nelson et al. 2002).

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